Roles of root border cells in plant defense and regulation of rhizosphere microbial populations by extracellular DNA 'trapping'

Plant and Soil

Volumn 355, Issue 1-2, 2012, Pages 1-16

  Hawes, Martha C ^a   Curlango Rivera, Gilberto ^a   Xiong, Zhongguo ^a   Kessler, John O ^b  

^a UNIVERSITY OF ARIZONA   (United States)

^b University of Arizona   (United States)

Author keywords

Extracellular DNA (exDNA); Mucilage; Rhizosphere colonization; Root border cells; Root cap; Root exudates

Indexed keywords

DNA; EXUDATION; HOST-PATHOGEN INTERACTION; IMMOBILIZATION; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; MUCILAGE; MUTATION; PLANT DEFENSE; PROTEIN; RHIZOSPHERE; ROOT COLONIZATION; ROOT SYSTEM; SOIL MICROORGANISM; TRAPPING; VIRULENCE;

ANIMALIA;

EID: 84858712004     PISSN: 0032079X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11104-012-1218-3     Document Type: Review

References (172)

1. Abdallah DS, Lin C, Ball CJ et al (2012) Toxoplasma gondii triggers release of human and mouse neutrophil extracellular traps. Infection Immun 80: 768-777.
2. Amulic B, Hayes G (2011) Neutrophil extracellular traps. Curr Biol 21: R297-R298.
3. Atkinson TG, Neal JL, Larson RI (1975) Genetical control of the rhizosphere of wheat. In: Bruehl GW (ed) Biology and control of soil-borne plant pathogens. American Phytopathological Society, St. Paul.
4. Bacic A, Moody SF, Clarke AE (1986) Structural analysis of secreted root slime from maize. Plant Physiol 80: 771-777.
5. Baluska F, Volkmann D, Hauskrecht M, Barlow PW (1996) Root cap mucilage and extracellular calcium as modulators of cellular growth in postmitotic growth zones of the maize root apex. Bot Acta 109: 25-34.
6. Bednarek P, Kwon C, Schulze-Lefert P (2010) Not a peripheral issue: secretion in plant-microbe interactions. Curr Opin Plant Biol 13: 378-385.
7. Bergsson G, Agerberth B, Jornvall H, Gudmundsson GH (2005) Isolation and identification of antimicrobial components from the epidermal mucus of Atlantic cod (Gadus morhua). FEBS J 272: 4960-4969.
8. Bowen GD, Rovira AD (1976) Microbial colonization of plant roots. Ann Rev Phytopathol 114: 121-144.
9. Bozhkov AI, Kuznetsova YA, Menzyanova NG (2007) Interrelationship between the growth rate of wheat roots, their excretory activity and the number of border cells. Russian J Plant Physiol 54: 97-103.
10. Brady NC, Weil RR (2010) Elements of the nature and properties of soils. Prentice Hall.
11. Brigham LA, Woo HH, Nicoll SM, Hawes MC (1995) Differential expression of proteins and messenger-RNAs from border cells and root tips of pea. Plant Physiol 109: 457-463.
12. Brigham LA, Woo HH, Wen F, Hawes MC (1998) Meristem-specific suppression of mitosis and a global switch in gene expression in the root cap of pea by endogenous signals. Plant Physiol 118: 1223-1231.
13. Brigham LA, Michaels PJ, Flores HE (1999) Cell-specific production and antimicrobial activity of naphthoquinones in roots of Lithospermum erythrorhizon. Plant Physiol 119: 417-428.
14. Brinkmann V, Zychlinsky A (2007) Beneficial suicide: why neutrophils die to make NETs. Nat Rev Microbiol 5: 577-582.
15. Brinkmann V, Brichard U, Goosmann C et al (2004) Neutrophil extracellular traps kill bacteria. Science 303: 1532-1535.
16. Brisson RF, Tenhaken R, Lamb C (1994) Function of oxidative cross linking of cell wall structural proteins in plant disease resistance. Plant Cell 6: 1703-1712.
17. Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco J (2008) Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol 74: 738-744.
18. Bruehl GW (1987) Soilborne plant pathogens. Macmillan Publishing Company, NY, USA.
19. Caffaro MM, Vivanco JM, Gutierrez BFH et al (2011) The effect of root exudates on root architecture in Arabidopsis thaliana. Plant Growth Regul 64: 241-249.
20. Cannesan MA, Gangneux C, Lanoue A et al (2011) Association between border cell responses and localized root infection by pathogenic Aphanomyces euteiches. Ann Bot 108: 459-469.
21. Caporali L (1983) Cytological study of cultured cells from maize root cap. Plant Sci Lett 31: 231-236.
22. Ceccherini MT, Ascher J, Agnelli A et al (2009) Experimental discrimination and molecular characterization of the extracellular soil DNA fraction. Antonie van Leeuwenhoek 96: 653-657.
23. Chaboud A, Rougier M (1990) Comparison of maize root mucilages isolated from root exudates and root surface extracts by complementary cytological and biochemical investigations. Protoplasma 156: 163-173.
24. Chen W, Liu P, Xu G et al (2008) Effects of aluminum on the biological characteristics of cowpea root border cells. Acta Physiol Plant 30: 303-308.
25. Clowes FAL (1971) The proportion of cells that divide in root meristems of Zea mays L. Ann Bot 35: 249-261.
26. Compant S, Duffy B, Nowak J et al (2005) Use of plant growth promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action and future prospects. Appl Environ Microbiol 71: 4951-4959.
27. Cooper JE, Rao JR eds (2006) Molecular approaches to soil, rhizosphere and plant microorganism analysis. CABI, Oxfordshire, UK, Cambridge MA, USA.
28. Curl EA, Truelove B (1986) The rhizosphere. Advanced series in agricultural sciences, vol. 15, Springer-Verlag, Berlin-Heidelberg-New York-Tokyo.
29. Curlango-Rivera G, Hawes MC (2011) Root tips moving through soil: an intrinsic vulnerability. Plant Signal Behavior 6: 1-2.
30. Curlango-Rivera G, Duclos DV, Ebolo JJ, Hawes MC (2010) Transient exposure of root tips to primary and secondary metabolites: impact on root growth and production of border cells. Plant Soil 332: 267-275.
31. Darrah PR, Roose T (2001) Modeling the rhizosphere. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil-plant interface. Marcel Dekker, Inc., New York, pp 327-372.
32. De-la-Pena C, Vivanco JM (2010) Root-microbe interactions: the importance of protein secretion. Curr Proteonomics 7: 265-274.
33. De-la-Pena C, Badri DV, Lei Z et al (2010) Root secretion of defense-related proteins is development-dependent and correlated with flowering time. J Biol Chem 285: 30654-30666.
34. Dennis PG, Miller AJ, Hirsch PR (2010) Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiol Ecol 72: 313-327.
35. Donato JJ, Moe LA, Converse BJ et al (2010) Metagenomic analysis of apple orchard soil reveals antibiotic resistance genes encoding predicted bifunctional proteins. Appl Environ Microbiol 76: 4396-4401.
36. Endo I, Tange T, Osawa H (2011) A cell-type-specific defect in border cell formation in the Acacia mangium root cap developing an extraordinary sheath of sloughed-off cells. Ann Bot 108: 279-290.
37. Esau K (1967) Plant anatomy. Wiley, New York.
38. Feldman LJ (1985) Root gravitropism. Physiol Plant 65: 341-344.
39. Foster RC (1981a) Polysacharrides in soil fabrics. Science 214: 665-667.
40. Foster RC (1981b) The ultrastructure and histochemistry of the rhizosphere. New Phytol 89: 263-273.
41. Foster RC (1982) The fine structure of epidermal cell mucilages of roots. New Phytol 91: 727-740.
42. Foster RC, Rovira AD, Cock TW (1983) Ultrastructure of the root-soil interface. American Phytopathological Society, St. Paul.
43. Fries N, Forsman B (1951) Quantitative determination of certain nucleic acid derivatives in pea root exudate. Physiol Plant 4: 410-420.
44. Gamalero E, Lingua G, Capri FG et al (2004) Colonization pattern of primary tomato roots by Pseudomonas fluorescens A6RI characterized by dilution plating, flow cytometry, fluorescence, confocal and scanning electron microscopy. FEMS Microbiol Ecol 48: 79-87.
45. Gamalero E, Lingua G, Tombolini R et al (2005) Colonization of tomato root seedling by Pseudomonas fluorescens 92rkG5: spatio-temporal dynamics, localization, organization, viability and culturability. Microbial Ecol 50: 289-297.
46. Gautheret MR (1933) Cultures of cells isolated from the root cap. CR Acad Sci 186: 638-640.
47. Gilbert GS, Clayton MK, Handelsman J, Parke JL (1996) Use of cluster and discriminant analysis to compare rhizosphere bacterial populations following biological perturbation. Microbial Ecol 32: 123-147.
48. Gochnauer MB, Sealey LJ, McCully ME (1990) Do detached root cap cells influence bacteria associated with maize roots? Plant Cell Environ 13: 793-801.
49. Goldberg NP, Hawes MC, Stanghellini ME (1989) Specific attraction to and infection of cotton root cap cells by zoospores of Pythium dissotocum. Can J Bot 67: 1760-1767.
50. Graham TC (1991) Flavonoid and isoflavonoid distribution in developing soybean seedling tissues and in seed and root exudates. Plant Physiol 95: 594-603.
51. Griffin GJ, Hale MG, Shay FJ (1975) Nature and quantity of sloughed organic matter produced by roots of axenic peanut plants. Soil Biol Biochem 8: 29-32.
52. Guinel FC, McCully ME (1986) Some water-related physical properties of maize root cap mucilage. Plant Cell Environ 9: 657-666.
53. Guinel FC, McCully ME (1987) The cells shed by the root cap of Zea: their origin and some structural and physiological properties. Plant Cell Environ 10: 565-578.
54. Gunawardena U, Hawes MC (2002) Tissue specific localization of root infection by fungal pathogens: role of root border cells. Mol Plant Microbe Int 15: 1128-1136.
55. Gunawardena U, Rodriguez M, Straney D et al (2005) Tissue specific localization of root infection by Nectria haematococca: mechanisms and consequences. Plant Physiol 137: 1363-1374.
56. Hamamoto L, Hawes MC, Rost TL (2006) The production and release of living root cap border cells is a function of root apical meristem type in dicotyledonous angiosperm plants. Ann Bot 97: 917-923.
57. Handelsman J (2004) Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mol Biol Rev 68: 669-685.
58. Handelsman J, Stabb EV (1996) Biocontrol of soilborne plant pathogens. Plant Cell 8: 1855-1869.
59. Harding M, Kubes P (2012) Innate immunity in the vasculature: interactions with pathogenic bacteria. Curr Opin Microbiol 15: 85-91.
60. Hawes MC, Wheeler H (1982) Factors affecting victorin-induced cell death: temperature and plasmolysis. Physiol Plant Pathol 20: 137-144.
61. Hawes MC, Pueppke SG (1986) Sloughed peripheral root cap cells: yield from different species and callus formation from single cells. Am J Bot 73: 1466-1473.
62. Hawes MC, Pueppke SG (1987) Correlation between binding of Agrobacterium tumefaciens by root cap cells and susceptibility of plants to crown gall. Plant Cell Rep 6: 287-290.
63. Hawes MC, Smith LY (1989) Requirement for chemotaxis in pathogenicity of Agrobacterium tumefaciens on roots of soil-grown pea plants. J Bacteriol 171: 5668-5671.
64. Hawes MC, Brigham LA (1992) Impact of root border cells on microbial populations in the rhizosphere. Adv Plant Pathol 8: 119-148.
65. Hawes MC, Smith LY, Howarth AJ (1988) Agrobacterium tumefaciens mutants deficient in chemotaxis to root exudates. Mol Plant Microbe Int 1: 182-186.
66. Hawes MC, Brigham LA, Wen F, Woo HH, Zhu Y (1998) Function of root border cells in plant health: pioneers in the rhizosphere. Ann Rev Phytopathol 36: 311-327.
67. Hawes MC, Gunawardena U, Miyasaka S, Zhao X (2000) The role of root border cells in plant defense. Trends Plant Sci 5: 128-133.
68. Hawes MC, Bengough G, Cassab G, Ponce G (2003) Root caps and rhizosphere. J Plant Growth Regul 21: 352-367.
69. Hawes MC, Curlango-Rivera G, Wen F et al (2011) Extracellular DNA: the tip of root defenses. Plant Sci 180: 741-745.
70. Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237: 173-195.
71. Hinsinger P, Brauman A, Devau N et al (2011) Acquisition of phosphorus and other poorly mobile nutrients by roots. Where do plant nutrition models fail? Plant Soil 348: 29-61.
72. Hirsch AM (2004) Plant-microbe symbioses: a continuum from commensalism to parasitism. Symbiosis 37: 345-363.
73. Humphris SN, Bengough AG, Griffiths BS et al (2005) Root cap influences root colonisation by Pseudomonas fluorescens SBW25 on maize. FEMS Microbiol Ecol 54: 123-130.
74. Iijima M, Griffiths B, Bengough AG (2000) Sloughing of cap cells and carbon exudation from maize seedling roots in compacted sand. New Phytol 145: 477-482.
75. Iijima M, Sako Y, Rao TP (2003) A new approach for the quantification of root cap mucilage exudation in the soil. Plant Soil 255: 399-407.
76. Izano EA, Amarante MA, Kher WB, Kaplan JB (2008) Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and S. epidermidis biofilms. Appl Environ Microbiol 74: 470-476.
77. Jaroszuk-Scisel J, Kurek E, Rodzik B, Winiarczyk K (2009) Interactions between rye (Secale cereale) root border cells (RBCs) and pathogenic and nonpathogenic rhizosphere strains of Fusarium culmorum. Mycol Res 113: 1053-1061.
78. Jones DD, Morre DJ (1973) Golgi apparatus mediated polysaccharide secretion by outer root cap cells of Zea mays. III. Control by exogenous sugars. Physiol Plant 29: 68-75.
79. Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant Soil 321: 5-33.
80. Kawasaki H, Iwamuro S (2008) Potential roles of histones in host defense as antimicrobial agents. Infect Disord Drug Targets 8: 195-205.
81. Knee EM, Gong FC, Gao MS et al (2001) Root mucilage from pea and its utilization by rhizosphere bacteria as a sole carbon source. Mol Plant Microbe Int 14: 775-784.
82. Knox OGG, Vadakattu GVSR (2005) Evaluation of border cell number and cry protein expression from root tips of Gossypium hirsutum. In: Cote JC, Otvos IS, Schwartz JL (eds) Pacific rim conference on the biotechnology of Bacillus thuringiensis and its environmental impact.
83. Knox OGG, Gupta VVSR, Nehl DB, Stiller WN (2007) Constitutive expression of cry proteins in roots and border cells of transgenic cotton. Euphytica 154: 83-90.
84. Knox OGG, Gupta VVSR, Lardner R (2009) Cotton cultivar selection impacts on microbial diversity and function. Aspects Appl Biol 98: 1-8.
85. Knudson L (1917) The toxicity of galactose and mannose for green plants and the antagonistic action of other sugars toward these. Am J Bot 4: 430-437.
86. Knudson L (1919) Viability of detached root cap cells. Am J Bot 6: 309-310.
87. Kraszewska EK, Bjerknes CA, Lamm SS, Van't Hopf J (1985) Extrachromosomal DNA of pea-root (Pisum sativum) has repeated sequences and ribosomal genes. Plant Mol Biol 5: 353-361.
88. Kubista M, Akerman B, Norden B (1987) Characterization of interaction between DNA and 4, 6-diamidino- 2- phenylindole by optical spectroscopy. Biochemistry 26: 4545-4553.
89. Kuzyakov YV (2001) Tracer studies of carbon translocation by plants from the atmosphere into the soil. Eurasian Soil Sci 34: 28-42.
90. Kwon C, Bednarek P, Schulze-Lefert P (2008) Secretory pathways in plant immune responses. Plant Physiol 147: 1575-1583.
91. Lagopodi AL, Ram AFJ, Lamers GEM et al (2002) Novel aspects of tomato root colonization and infection by Fusarium oxysporum f. sp radicis-lycopersici revealed by confocal laser scanning microscopic analysis using the green fluorescent protein as a marker. Mol Plant Microbe Int 15: 172-179.
92. Lee A, Hirsch AM (2006) Signals and responses: choreographing the complex interaction between legumes and alpha- and beta-rhizobia. Plant Signal Behavior 1: 161-168.
93. Levy-Booth DJ, Campbell RG, Gulden RH et al (2007) Cycling of extracellular DNA in the soil environment. Soil Biol Biochem 39: 2977-2991.
94. Liu B, Zeng Q, Yan F et al (2005) Effects of transgenic plants on soil microorganisms. Plant Soil 271: 1-13.
95. Liu J, Yu M, Wang W, Feng Y (2007) Influence of boron and aluminum on production and viability of root border cells of pea. Adv Plant Animal Boron Nutrition, pp 67-74.
96. Loh J, Pierson EA, Pierson LS III, Stacy G, Chatterjee A (2002) Quorum sensing in plant-associated bacteria. Curr Opin Plant Biol 5: 1-5.
97. Lundegarth H, Stenlid G (1944) On the exudation of nucleotides and flavonone from living roots. Arkiv f Bot 31A: 10.
98. Luster J, Gottlein A, Nowack B, Sarret G (2009) Sampling, defining, characterizing and modeling the rhizosphere-the soil science tool box. Plant Soil 321: 457-482.
99. Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129: 1-10.
100. Lynch MA, Staehelin LA (1995) Immunocytochemical localization of cell wall polysaccharides in the root tip of Avena sativa. Protoplasma 188: 115-127.
101. Marschner P, Crowley D, Rengel Z (2011) Rhizosphere interactions between microorganisms and plants govern iron phosphorus acquisition along the root axis-model and research methods. Soil Biol Biochem 43: 883-894.
102. Matsuyama T, Satoh H, Yamada Y, Hashimoto T (1999) A maize glycine-rich protein is synthesized in the lateral root cap and accumulates in the mucilage. Plant Physiol 120: 665-674.
103. Maxwell CA, Phillips DA (1990) Concurrent synthesis and release of nod gene inducing flavonoids from alfalfa roots. Plant Physiol 93: 1552-1558.
104. McDougall BM, Rovira AD (1970) Sites of exudation of C-14-labelled compounds from wheat roots. New Phytol 69: 999.
105. Medina E (2009) Neutrophil extracellular traps: a strategic tactic to defeat pathogens with potential consequenes for the host. J Innate Immun 1: 176-179.
106. Miki NK, Clarke KJ, McCully ME (1980) A histological and histochemical comparison of the mucilages on the root tips of several grasses. Can J Bot 58: 2581-2593.
107. Mitroulis I, Kambas K, Chrysanthopoulou A et al (2011) Neutrophil extracellular trap formation is associated with IL-1beta and autophagy-related signaling in gout. PLoS One 6: e29318.
108. Miyasaka S, Hawes MC (2001) Possible role of root border cells in detection and avoidance of aluminum toxicity. Plant Physiol 125: 1978-1987.
109. Moody SF, Clarke AE, Bacic A (1988) Structural analysis of secreted slime from wheat and cowpea roots. Phytochemical 27: 2857-2861.
110. Moore R, Fondren WM (1986) The possible involvement of root-cap mucilage in gravitropism and calcium movement across root tips of Allium cepa L. Ann Bot 58: 381-387.
111. Morris CE, Monier J-M (2003) The ecological significance of biofilm formation by plant-associated bacteria. Ann Rev Phytopathol 41: 429-453.
112. Newcomb EH (1967) Fine structure of protein-storing plastids in bean root tips. J Cell Biol 33: 143-163.
113. Oades JM (1978) Mucilage at the root surface. J Soil Sci 29: 1-16.
114. Odell RE, Dumlao MR, Samar D, Silk WK (2008) Stage-dependent border cell and carbon flow from roots to rhizosphere. Am J Bot 95: 441-446.
115. Pan J, Ye D, Wang L et al (2004) Root border cell development is a temperature-insensitive and Al-sensitive process in barley. Plant Cell Physiol 45: 751-760.
116. Park SJ, Pai KS, Kim JH, Shin JI (2012) ANCA-associated glomerulonephritis in a patient with infections endocarditis: the role of neutrophil extracellular traps? Revue Med Int 33: 57.
117. Patat SA, Carnegie RB, Kingsbury C et al (2004) Antimicrobial activity of histones from hemocytes of the pacific white shrimp. Eur J Biochem 271: 4825-4833.
118. Patel S, Kumar S, Jyoti A et al (2010) Nitric oxide donors release extracellular traps from human neutrophils by augmenting free radical generation. Nitric Oxide 22: 226-234.
119. Peters NK, Long SR (1988) Alfalfa root exudates and compounds which promote or inhibit induction of Rhizobium meliloti nodulation genes. Plant Physiol 88: 396-400.
120. Phillips HL, Torrey JG (1971) Deoxyribonucleic acid synthesis in root cap cells of cultured roots of Convolvulus. Plant Physiol 48: 213-218.
121. Pierson LS III, Pierson EA (2007) Roles of diffusible signals in communication among plant-associated bacteria. Phytopathology 97: 227-232.
122. Pietramellara G, Ascher J, Borgogni F et al (2009) Extracellular DNA in soil and sediment: fate and ecological relevance. Biol Fertil Soils 45: 219-235.
123. Pilszik FH, Salina D, Poon KK et al (2010) A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus. J Immunol 185: 7413-7425.
124. Pinton R, Varanini Z, Nanipieri P, eds (2007) The rhizosphere: biochemistry and organic substances at the soil-plant interface. Marcel Dekker, Inc. New York, Basel.
125. Ponce G, Barlow PW, Feldman LJ, Cassab GI (2005) Auxin and ethylene interactions control mitotic activity of the quiescent centre, root cap size, and pattern of cap cell differentiation in maize. Plant Cell Environ 28: 719-732.
126. Read DB, Gregory PJ, Bell AE (1999) Physiological properties of axenic maize root mucilage. Plant Soil 211: 87091.
127. Rogers HT, Pearson RW, Pierre WH (1942) The source and phosphatase activity of exoenzyme systems of corn and tomato roots. Soil Sci 54: 353-365.
128. Rovira AD (1969) Plant root exudates. Bot Rev 35: 35-57.
129. Rovira AD (1991) Rhizosphere research: 85 years of progress and frustration. In: Keister DL, Cregan PB (eds) The rhizosphere and plant growth. Kluwer, Dordrecht, pp 3-13.
130. Saxena D, Stotzky G (2001) Bacillus thuringiensis (Bt) toxin released from root exudates and biomass of Bt corn has no apparent effect on earthworms, nematodes, protozoa, bacteria, and fungi in soil. Soil Biol Biochem 33: 1225-1230.
131. Schroth MN, Snyder WC (1961) Efect of host exudates on chlamydospore germination of the bean root rot fungus Fusarium solani f sp phaseoli in soil. Phytopathology 52: 279-285.
132. Sealey LJ, McCully ME, Canny MJ (1995) The expansion of maize root cap mucilage during hydration. I. Kinetics. Physiol Plant 93: 38-46.
133. Sherwood RT (1987) Papilla formation in corn root cap cells and leaves inoculated with Colletotrichum graminicola. Phytopathology 77: 930-934.
134. Smucker AJM, Erickson AE (1987) Anaerobic stimulation of root exudates and disease of peas. Plant Soil 99: 423-433.
135. Somasundaram S, Fukuzono S, Iijima M (2008) Dynamics of root border cells in rhizosphere soil of Zea mays L.: crushed cells during root penetration, survival in soil, and long term soil compaction effect. Plant Prod Sci 11: 440-446.
136. Stenlid G (1944) Physicochemical properties of the surface of growing plant cells. Nature 153: 618-619.
137. Stubbs VEC, Standing D, Knox OGG et al (2004) Root border cells take up and release glucose-C. Ann Bot 93: 221-224.
138. Sylvia DM, Fuhrmann JJ, Hartel PG, Zuberer DA (1998) Principles and applications of soil microbiology. Prentice Hall, USA.
139. Tamas L, Budikova S, Huttova J et al (2005) Aluminum-induced cell death of barley root border cells is correlated with peroxidase and oxalate oxidase-mediated hydrogen peroxide production. Plant Cell Rep 24: 189-194.
140. Tapp H, Stotzky G (1997) Monitoring the fate of insecticidal toxins from Bacillus thuringiensis in soil with flow cytometry. Can J Microbiol 43: 1074-1078.
141. Urban CF, Lourido S, Zychlinsky A (2006) How do microbes evade neutrophil killing? Cell Microbiol 8: 1687-1696.
142. Uren NC (2001) Types, amounts, and possible functions of compounds released into the rhizosphere by soil-grown plants. In: Pinton R, Varanini P, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil-plant interface. Marcel Dekker, Inc., New York, Basel. pp 19-40.
143. van Egeraat AWSM (1975) Exudation of ninhydrin-positive compounds by pea seedling roots: a study of the sites of exudation and of the composition of the exudate. Plant Soil 42: 37-47.
144. Van't Hopf J, Bjerknes CA (1982) Cells of pea (Pisum sativum) that differentiate from G2 phase have extrachromosomal DNA. Mol Cell Biol 2: 339-345.
145. Vermeer J, McCully ME (1982) The rhizosphere in Zea: new insight into its structure and development. Planta 156: 45-61.
146. Vicre M, Santaella C, Blanchet S, Gateau A, Driouich A (2005) Root border like cells of Arabidopsis. Microscopical characterization and role in the interaction with rhizobacteria. Plant Physiol 138: 998-1008.
147. Vlassov VV, Laktionov PP, Rykova EY (2007) Extracellular nucleic acids. Bioessays 29: 654-667.
148. Voeller BR, Ledbetter MC, Porter KR (1964) The plant cell: aspects of its form and function. In: Bracket J, Minsky EE (eds) The cell, vol 6. Academic, London, pp 245-312.
149. Wang Y, Li M, Stadler S, Correll S et al (2009) Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J Cell Biol 184: 205-213.
150. Wardini AB, Guimaraes-Costa AB, Nascimento MT et al (2010) Characterization of neutrophil extracellular traps in cats naturally infected with feline leukemia virus. J Gen Virol 91: 259-264.
151. Watt M, McCully ME, Jeffree CE (1993) Plant and bacterial mucilages of the maize rhizosphere: comparison of their soil binding properties and histochemistry in a model system. Plant Soil 151: 151-165.
152. Watt M, Silk WK, Passioura J (2006) Rates of root and organism growth, soil conditions and temporal and spatial development of the rhizosphere. Ann Bot 97: 839-855.
153. Weller DM (1988) Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annu Rev Phytopathol 26: 379-407.
154. Wen F, Zhu Y, Brigham LA, Hawes MC (1999) Expression of an inducible pectinmethylesterase gene is required for border cell separation from roots of pea. Plant Cell 11: 1129-1140.
155. Wen F, Curlango-Rivera G, Hawes MC (2007a) Proteins among the polysaccharides: a new perspective on root cap slime. Plant Signal Behavior 2: 1-3.
156. Wen F, VanEtten HD, Tsaprailis G, Hawes MC (2007b) Extracellular proteins in pea root tip and border cell exudates. Plant Physiol 143: 773-783.
157. Wen F, Woo HH, Pierson EA et al (2008) Synchronous elicitation of development in root caps induces transient gene expression changes common to legume and gymnosperm species. Plant Mol Biol Rep 27: 58-68.
158. Wen F, White GJ, VanEtten HD et al (2009) Extracellular DNA is required for root tip resistance to fungal infection. Plant Physiol 151: 820-829.
159. Wen F, Shen A, Choi A, Shi J (2012) A xenograft pancreatic cancer mouse model to study the function of extracellular DNA in metastasis. Proceedings, American Association of Cancer Research.
160. Whipps J, Lynch JM (1983) Substrate flow and utilization in the rhizosphere of cereals. New Phytol 95: 605-623.
161. Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS (2002) Extracellular DNA required for bacterial biofilm formation. Science 295: 1487.
162. Woo HH, Hirsch AM, Hawes MC (2004) Altered susceptibility to infection by Sinorhizobium meliloti and Nectria haematococca in alfalfa roots with altered cell cycle. Plant Cell Rep 12: 967-973.
163. Wood RKS (1967) Physiological plant pathology. Blackwell, Oxford.
164. Wuyts N, Maung ZTZ, Swennen R, De Waele D (2006) Banana rhizodeposition: characterization of root border cell production and effects on chemotaxis and motility of the parasitic nematode Radopholus similis. Plant Soil 283: 217-228.
165. Xu J, Zhang X, Pelayo R, Monestier M et al (2009) Extracellular histones are major mediators of death in sepsis. Nat Med 15: 1318-1321.
166. Yost CC, Cody MJ, Harris ES et al (2009) Impaired NET formation: a novel innate immune deficiency of human neonates. Blood 113: 6419-6427.
167. Young RL, Malcolm KC, Kret JE, Caceres SM et al (2011) Neutrophil extracellular trap (NET)-mediated killing of Pseudomonas aeruginosa: evidence of acquired resistance within the cystic fibrosis airway, independent of CFTR. PLoS One 6: e23637.
168. Zentmyer G (1963) Biological control of Phytophthora root rot of avocado with alfalfa meal. Phytopathology 53: 1383.
169. Zhao X, Misaghi IJ, Hawes MC (2000) Stimulation of border cell production in response to increased carbon dioxide levels. Plant Physiol 122: 181-188.
170. Zhu M, Ahn S, Matsumoto H (2003) Inhibition of growth and development of root border cells in wheat by Al. Physiol Plant 117: 359-367.
171. Zhu Y, Pierson LS, Hawes MC (1997) Induction of microbial genes for pathogenesis and symbiosis by chemicals from root border cells. Plant Physiol 115: 1691-1698.
172. Zobel RW, Wright SF (2005) Roots and soil management: interactions between roots and the soil. American Society of Agronomy, Inc., Crop Science Society of America, Inc., Soil Science Society of America, Inc. Madison WI, USA.